Canadian Landscape Assessment of Colorectal Cancer Screening during the COVID-19 Pandemic

Response to Reviewer 1 Comments

1. Summary

Thank you very much for taking the time to review this manuscript. I can see from the tremendous work you’ve put in your comments and suggestions that you’re very passionate about ensuring the manuscript is comprehensive in all aspects. Please find the detailed responses below and the corresponding revisions/corrections highlighted in track changes in the re-submitted files.

2. Comments and Suggestions for Authors:

Response and Revisions

1. While the article mentions the impact of delayed screenings, could you please elaborate on the potential consequences for treatment outcomes in patients whose colorectal cancer diagnoses were delayed? What impact might delayed staging have on treatment decisions and patient prognosis?

2.     Although the article discusses the decline in colorectal cancer screenings, could you provide insight into the statistical methods used to estimate missed screenings and potential future burden? When interpreting these estimates, what level of uncertainty should decision-makers consider?

3.     The article discusses strategies for mitigating future disruptions; could you elaborate on how these strategies align with broader public health goals and priorities? What can be learned from this pandemic to help build a more resilient and adaptable healthcare system?

4.     The article mentions prioritizing high-risk patients, but could you go into more detail about the ethical considerations in making these decisions? How can equity be maintained while vulnerable populations are prioritized for screenings and procedures?

5.     You mentioned patient hesitancy; could you elaborate on the psychological factors that influence people's decisions to resume screenings? How can behavioral interventions be tailored to overcome specific barriers and encourage patients to prioritize their colorectal health?

6.     The article mentions changes in screening program invitations briefly, but could you elaborate on how medical education can be adapted to provide healthcare providers with the skills to effectively communicate the importance of colorectal cancer screenings in a post-pandemic landscape?

7.     The article discusses backlog-reduction strategies; could you expand on the potential policy implications of these strategies? How do these strategies fit into the broader goals and priorities of healthcare policy?

8.     While the article focuses on healthcare, could you share your insights into the patient experience during this disruption? What suggestions do you have for patient advocacy groups to help individuals who have had screenings and treatments delayed?

9.     The article mentions the need for improved data collection; however, could you explain how quality improvement initiatives can be implemented to improve data accuracy, reporting, and analysis in colorectal cancer screening programs?

10.   The article mentions the use of technology, but could you go into more detail about how emerging health technologies, such as wearable devices and remote monitoring, could help with colorectal cancer prevention and patient engagement?

11.            Effective communication is critical in persuading patients to return for screenings. Could you give some examples of creative communication strategies that have been successful in assuaging patients' concerns about safety protocols and motivating them to prioritize colorectal cancer screenings?

12.   While the article briefly  mentioned the cost implications of disruptions, could you shed some light on the long-term economic implications of delayed colorectal cancer diagnoses? How do these costs stack up against the investments needed for a comprehensive recovery strategy?

1. Thank you for bringing this point forward. I agree it’s important to consider the possible consequences for patients whose CRC diagnoses were delayed. In the article it is noted that “regular screenings to help detect CRC in its earliest, most curable stages.” And stage shifting due to delays would “would result in upstaging as more patients would progress from stage I to stage IV carcinomas.”, which would unfortunately this would lead to a poorer prognosis and chance of survival. I have made the necessary changes in the manuscript (see tracked changes on page 2, section 1 in re-submitted file).

2. All of statistics from the results were obtained from the survey and analyzed descriptively to assess the proportions in the number of missed CRC screenings for both FIT and colonoscopy. The level of uncertainty decision-makers is contingent on the utility of these percentages. As the provided numbers from P/Ts varied on the time range and type of CRC screening they reported (e.g., FIT and/or colonoscopy).

3. These strategies were developed by utilizing the responses provided by the P/Ts and assessing what common themes emerged from their responses. These strategies align with the various provincial and territorial representatives’ public health goals, and they have been reviewed by the Canadian Partnership Against Cancer (CPAC) to ensure they align with their broader public health goals and current initiatives. Moreover, there are various lessons that can be learned from the pandemic (which are highlighted in this manuscript), such as better planning (e.g., creating a contingency plan) and having the capacity and ability to more collect more comprehensive data (e.g., having adequate data for guiding the triage of CRC screening services and delayed patients). Also, other important considerations, in regard to CRC include accessibility/resources for FIT (e.g., FIT kits available in health centres) and having the human resources to complete follow-up colonoscopies.

4. This recommendation is included in the manuscript, as some P/T representatives highlighted this consideration for addressing the backlog of CRC screening/procedures. For example, the Quebec representative noted that they used a prioritization framework within in their colonoscopy request form with five priority levels based on a risk assessment of morbidity and mortality outcomes. The equity considerations for each P/T would differ based on what type of prioritization framework they are using (if they have one) and their specific equity, diversity, and inclusion (EDI) principles. Accordingly, this research would have to be expanded to assess how equity could be maintained while dealing with vulnerable populations. I would be interested to follow-up on this matter with the P/T representatives in a future study.

5. Yes, there were articles noting that a decrease in cancer screening could be due to fear of exposure to the virus or other concerns (e.g., overburdening the healthcare system) during the pandemic. This was included in this manuscript on page 2. Although, regarding the psychological factors involved in resuming screening, this is not explicitly noted, but it has been considered. In the manuscript, you will find that CRC screening awareness campaigns are highlighted, and this is to increase screening and reduce the aforementioned fears. Although, to ensure this important topic is clearly highlighted, I have revised the manuscript (see tracked changes on page 14, section 4.1 in re-submitted file).

6. That’s an important aspect to consider, since healthcare providers need to be knowledgeable in communicating CRC screening with their patients. This aspect is something that Colorectal Cancer Canada has considered and is working towards in our advocacy/awareness initiatives, such as toolkit development targeted towards healthcare providers. Also, addressing increasing resources in the healthcare system by deploying patient navigators/community health liaisons could assist in communicating the importance of CRC in the post-pandemic landscape (see revised statement on page 14, section 4.1).

7. Yes, there are various backlog-reduction strategies that were provided based on the responses provided by the P/T representatives. The policy implications of these strategies would vary for each jurisdiction, especially since each P/T has different priorities, strategies, and political agendas. Accordingly, I would have follow-up with the P/T representatives to accurately assess the policy implications based on their suggested strategies for addressing the backlog of CRC screening (with FIT and colonoscopies). Also, as aforementioned these strategies align with the various provincial and territorial representatives’ public health goals, and they have been reviewed by the Canadian Partnership Against Cancer (CPAC) to ensure they align with their broader public health goals and current initiatives.

8. I completely agree that it is significant to explore patients’ experiences during this disruption. Although, this study primarily explores the impact of the pandemic on CRC screening from the perspective of P/T representatives. I think it would be interesting to have a follow-up study or systematically review existing studies exploring the insights of patients during this disruption. For patient advocacy groups, such as Colorectal Cancer Canada, it is important for us to advocate for better solutions within the healthcare system, such as providing accessible FIT (e.g., available in pharmacies and mailing FIT kits in all P/Ts) and advocating for policy change by sharing this study with policymakers.

9. Yes, data collection was a barrier to not only getting representative data from the P/T representatives, but adequately quantifying the impact of COVID-19 on CRC screening. As mentioned in the recommendations section, “having a more efficient data collection system that allows for timely and accurate data accessible to researchers and policymakers.” is important to consider. It is important to further investigate this challenge and assess which quality improvement initiatives are necessary to accurately collect comprehensive data for CRC screening programs. see tracked changes on page 16, section 4.4 in re-submitted file).

10. The key solutions and recommendations from the P/T representatives did not focus on innovative technologies, which is why it’s not discussed in detail in this study. However, wearable health technologies/devices are important for monitoring various diseases, such as CRC, it is not a focus for this study. Although, I do think this is an important topic for Colorectal Cancer Canada to consider for future research initiatives.

11. I completely agree that effective communication is instrumental in persuading patients to return to screenings. In this study, the P/T representatives discussed the significance of utilizing awareness initiatives/communication strategies, such as public health campaigns (see section 3.5.3) and mailing FIT kits (see section 3.9.2) to mitigate the impact of the pandemic. These methods are important for influencing individual behaviours and increasing adherence to CRC screening. Also, it is important to assess in more detail, what type of messaging the P/T were including, and are currently including in their public health campaigns/FIT mailing kits/reminders letter. For example, in section 3.9.2, it is noted that Prince Edward Island mentioned that “public messaging is important for promoting support and developing confidence for CRC screening, including messaging highlighting the appropriateness and importance of CRC screening even during a pandemic.”

12. This study noted how these disruptions could lead to stage shifting, and consequently, increased morbidities and mortalities. Also, the recommendations section noted that additional funding is needed to increase the capacity of CRC screening services. While long-term economic implications are significant to explore, this study did not explicitly this topic; which is why I’m hesitant to expand on this aspect in the discussion, main findings, or other sections. Although, I do agree that exploring this health economic topic is important, such as assessing the implications and investments needed for a comprehensive recover strategy. Future studies (e.g., exploring cost-effectiveness of a recovery strategy) are needed to better assess how P/T should proceed and whether they already have plans in place to recover (note. this study noted a few recovery strategies shared by P/T representatives, such as COVID-19 recovery plans).

3. Point-by-point response to Comments on the Quality of English Language:

Comments 1: Excerpt 1 (Introduction):

The COVID-19 pandemic introduced a multitude of challenges to the cancer care delivery system. Colorectal cancer prevention and diagnostic tests such as fecal immunochemical tests (FIT) and colonoscopies declined dramatically during the first wave of the pandemic. Since then, the cancer control communities across provinces have struggled to quantify the amount of missing screening, procedures and cancer diagnoses.

My Revision: The onset of the COVID-19 pandemic ushered in an array of challenges for the cancer care delivery system. Notably, preventive and diagnostic measures for colorectal cancer, including fecal immunochemical tests (FIT) and colonoscopies, experienced a significant decline during the initial pandemic wave. In the aftermath, the various cancer control communities spanning provinces have encountered difficulties in accurately quantifying the extent of screening deficits, procedural interruptions, and cancer diagnoses that were missed.

Response 1: I agree that the revised version is much more clear. Although, I will not be able to use the revised version, as this excerpt is from the questionnaire provided in Appendix A. I must keep the questionnaire as it was originally shared with the provincial and territorial representatives.

Comments 2:

Excerpt 2: The COVID-19 pandemic introduced a multitude of challenges to the cancer care delivery system. Colorectal cancer prevention and diagnostic tests such as fecal immunochemical tests (FIT) and colonoscopies declined dramatically during the first wave of the pandemic. Since then, the cancer control communities across provinces have struggled to quantify the amount of missing screening, procedures and cancer diagnoses.

My Revision: The COVID-19 pandemic has posed numerous challenges to the cancer care delivery system. Colorectal cancer prevention and diagnostic tests, including fecal immunochemical tests (FIT) and colonoscopies, experienced a significant decline during the initial wave of the pandemic. Subsequently, cancer control communities across provinces have faced difficulties in quantifying the extent of missed screenings, procedures, and cancer diagnoses.

Response 2: This is the same excerpt from Appendix A, see aforementioned response. Again, I appreciate you providing options for revising this excerpt.

Comments 3:

Excerpt 3 (Introduction):

Our study has found several intervention measures that can be used to make CRC screening programs more accessible and resilient.

My Revision: Our study has unearthed several intervention measures that possess the potential to render CRC screening programs more accessible and resilient.

Response 3: I agree with your revision, and have made the necessary changes (see attached revised document, page 16, section 4.5).

Comments 4:

Excerpt 4 (Introduction):

The study results also emphasize the necessity of having easily available information and expanded healthcare system resources to help mitigate the effects of the pandemic on screening.

My Revision: Furthermore, the outcomes of the study underscore the imperative nature of readily accessible information and augmented resources within the healthcare system, instrumental in mitigating the repercussions of the pandemic on the screening process.

Response 4: I agree with your revision and have made the necessary changes (see attached revised document, page 16, section 4.5).

Comments 5:

Excerpt 5 (Discussion):

By prioritizing high-risk populations and implementing flexible screening programs, healthcare providers and organizations can make CRC screening programs more resilient to withstand disruptions caused by a pandemic or other public health emergency.

My Revision: By according priority to high-risk populations and instituting adaptable screening programs, healthcare providers and organizations can bolster the resilience of CRC screening initiatives, rendering them more capable of weathering disruptions stemming from pandemics or other public health crises.

Response 5: I agree with your revision and have made the necessary changes (see attached revised document, page 15, section 4.1).

Comments 6:

Excerpt 6 (Discussion):

Our study also found that dealing with the consequences of the pandemic on CRC screening services necessitates a multi-faceted approach that includes prioritization, intersectoral collaboration and communication, awareness campaigns, financial support, and addressing future research concerns.

My Revision: Our investigation further revealed that effectively addressing the aftermath of the pandemic's impact on CRC screening services mandates a multifaceted strategy, encompassing prioritization, collaborative efforts across sectors, enhanced communication, targeted awareness campaigns, financial backing, and the resolution of impending research challenges.

Response 6: I agree with your revision and have made the necessary changes (see attached revised document, page 17, section 4.5).

Comments 7:

Excerpt 7 (Discussion):

Despite these limitations, the insights from this study may help inform policymaking to improve the accessibility and resilience of CRC screening programs in Canada.

My Revision: In spite of these limitations, the revelations garnered from this study can serve as valuable inputs for policy formulation, enabling enhancements in the accessibility and robustness of CRC screening programs across Canada.

Response 7: I agree with your revision and have made the necessary changes (see attached revised document, page 16, section 4.3).

Response to Reviewer 2 Comments

1. Summary

Thank you very much for taking the time to review this manuscript. Please find the detailed responses below and the corresponding revisions/corrections highlighted in track changes in the re-submitted file.

1.     Introduction. Well written and easy to follow. Grammatical error “Moreover, another 20% drop in diagnostic from the current levels would still trigger a further 7.2% increase in upstaging of the carcinomas [13]” diagnosis? or diagnostic what? Missing full stop: Earlier access to urgent catch-up screenings by screening and diagnostic institutions could mitigate the forecasted adverse outcomes or even eliminate them [4]The impact

Response #1: Thank you for bringing these grammatical errors forward. I have corrected them, see tracked changes on page 2, section 1 (introduction).

2.     Methods/Results: It is not clear to me why certain provinces/territories provided more than one response. How many CCC representatives does each province/territory have? Why not just send the invite to one representative for each province/territory?

Response #2: The P/T representatives were contacted from the National Colorectal Cancer Screening Network (NCCSN). Accordingly, multiple representatives were contacted to ensure each P/T had adequate representation, just incase one individual did not respond or provided incomplete responses.

3.     Suspension of screening services varied widely from 4 weeks to 24 weeks it would interesting to explore why there was such a difference.

Response #3: Agreed, it would have been interesting to explore this issue in-depth. One reason I found was a huge contributor was the lack of adequate data collection, and consistent and comprehensive available data from each P/T.

4.     3.4 Missed colorectal screening: data is reported in many different ways making understanding and comparison difficult for the reader. I wonder if a table showing percentage reductions in FIT and colonoscopy uptake might be more informative?

Response #4: I agree it may be difficult to follow, since each P/T had a different way of reporting how CRC screening was measured. I believe initially we did have a table, but agreed it made it even more complicated to understand since there wasn’t a consistent measure.

5.     Pagination needs to be addressed by journal editorial team for example titles for figure 4 and figure 6 are on the wrong page

Response #5: Is there anything I can do to correct this on my end?

6.     The problems and solutions in this paper are specific to Canada and highlight variations in screen programmes between the provinces and territories. I am not sure how relevant/interesting this would be to a worldwide readership. For example I find it odd that FIT samples are not automatically posted to the individual and returned by post (which is routine and current practice in my healthcare setting). Similarly other healthcare environments moved to exclusively using FIT during the COVID pandemic and have shown they can significantly reduce the number of subsequent colonoscopies required and are now employing this strategy in the their post pandemic practise. [for example Hunt N, Rao C, Logan R, et al. A cohort study of duplicate faecal immunochemical testing in patients at risk of colorectal cancer from North- West England. BMJ Open 2022;12:e059940. doi:10.1136/ bmjopen-2021-059940 ]

Response #6: This article is more so tailored to the Canadian audience and policymakers within Canada, rather than globally (which is also important to consider). Global leaders/researchers can still utilize this information as a comparison, to see for example how well they are performing against Canada. Also, I agree the FIT variation across Canada is odd, and some P/T are trying to adjust, as noted by PEI (section 3.6.1). Thank you for sharing the Hunt et al. study, it’s interesting to see healthcare environments are shifting to use exclusively FIT, especially during the pandemic. Although, I think a challenge with this approach could be whether the patient is at average risk for CRC or high-risk, since high-risk patients may be directly recommended to get a colonoscopy. Most screening initiatives such as FIT in Canada are targeted towards average risk patients. Also, interestingly, the threshold for a positive FIT varies among Canadian provinces and territories (https://www.partnershipagainstcancer.ca/topics/colorectal-cancer-screening-in-canada-2021-2022/fecal-testing/), so the sensitivity and specificity of the test would vary.

7.     Implementing measures to encourage individuals without a PCP or access to regular follow-up to participate in CRC screening by allowing other authorized HCPs to initiate screening. I am not sure what PCP or HCP stand for please expand.

Response 7: (PCPs) are primary care providers, such as family doctors/family physicians (see section 3.5.3, where term is first used). While HCPs are healthcare providers, and encompass family doctors, nurse practitioners, oncologists, etc. (see section 4, where term is first used).

8.     Additional funding. I am not convinced that a call for increased resources in the discussion has been justified particularly in the light of data that has shown that better stratification can actually decrease resource requirements (see previous ref).

Response 8: I agree it could be difficult to justify additional funding without further research. This suggestion, along with others, was recommended on the premise of what the provincial and territorial representatives were suggesting (see section 3.5.4). Also, additional funding could still be important to consider, especially during the time of this study, since there was backlog/disruptions/delays, and increasing humans resources to support screening services could help mitigate some of these challenges.

Response to Reviewer 3 Comments

1. Summary

Thank you very much for taking the time to review this manuscript. Please find the detailed responses below. Note, a revised corresponding document was not necessary for this review.

1.     1. Introduction - Sets scene well

Response #1: Thank you, I appreciate your kind feedback.

2.     Methods -

(1) Does the NCCSN include all potential stakeholders

(2) Were any excluded groups/ parties ?

(3) How did you ensure enrollment and recruitment

(4) Was data anonymized  ? - assume not

Response #2: (1) Yes the NCCSN includes all key stakeholders relevant for this study and they work closely with the Canadian Partnership Against Cancer (CPAC). (2) No key groups were excluded. (3) As mentioned in section 2.3.1, “The survey was disseminated via email on May 13, 2022, followed by weekly follow-up emails and one phone call until all NCCSN members of provincial and territorial screening programs were represented.” and CPAC assisted as well. (4) The numerical responses were aggregated and data was not anonymized, as some of the provincial and territorial representatives were thanked in the acknowledge.

3.     Results:

(1) Do we have any idea of volume disruptions in % by each areas

(2) What strategies to mitigate were undertaken ? - More FIT testing, public-private interventions, out-sourcing, use of radiology/ capsule endoscopy etc

(3) Do we have details on difference in suspension time - State/province led or at national level ?

(4) What were delays for the "RED" flag population - requiring urgent scopes

(5) What has been the real-world impact - up-surge in cancer diagnosis during and post Covid - Stage migration of advanced tumors ?

(6) In "catch-up" phase what initiatives are happening - National outsourcing to other regions or private sector

Response #3: (1) No, I do not have data about the volume of disruptions in % by each areas. It seems difficult to gather consistent and comprehensive data, due to the different methods used by provinces and territories. (2) Various strategies were undertaken to mitigate prioritization and targeting high-risk patients, intersectoral collaboration and communication, CRC screening awareness campaigns, financial support to increase capacity, and future research considerations (see section 3.5). For example, Quebec also noted that additional funding was made available to fund additional human resources and increase the capacity for colonoscopies beyond the previous base-line year 2019 (section 3.5.4). (4) Regarding the details on the difference in suspension time, unfortunately we do not have those specific details, especially at the national level. The provinces and territories varied in which services (e.g., FIT and/or colonoscopy) they included in their reported suspension time. (4) I don’t have the percentages for the “red” flag population, but I agree that it’s an important topic to explore. The provincial and territorial representatives noted that they prioritized high-risk patients (e.g., those with a positive FIT), and each had a different method/framework for how they prioritized these individual (see section 3.5.1). (5) Exploring the “real world impact” is very important should be monitored. One study that was included in our introduction (section 1) noted that “if the healthcare system fails to contain the ongoing reductions in diagnostic procedures, then 6.4% of CRC cases would exhibit greater stage shifting [13].” (6) In the “catch-up phase reported in this study, some provinces and territories noted first that they did have plan (see figures 3 and 4) and noted the average time it would take them to “catch-up on overdue FIT and colonoscopies (see figure 5). Although, regarding the specific strategies, some noted they had already “caught up” through resuming endoscopy services (Nova Scotia), while others, such as noted that had a plan to catch-up on colonoscopies based on FIT-positive data and procedures that could be accessed in each endoscopy unit. This area needs further investigation, but the Canadian Partnership Against Cancer (CPAC) and the NCCSN do post regular updates about their initiatives (which I’m not sure if I can share, since it’s included in their responses) and they have ongoing activities planned.

4.     Discussion - Overall clear message

Need to acknowledge lack of hard data on knock-on effect in terms of stage migration cancers, other pathologies etc

Response #4: Thank you, I agree it’s important to address all of these aspects.

5.     Figures/Tables - No issues

Response #5: Thank you.